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Title Tooth size variation in pinniped dentitions

Author(s) Wolsan, Mieczyslaw; Suzuki, Satoshi; Asahara, Masakazu;Motokawa, Masaharu

Citation PLOS ONE (2015), 10(8)

Issue Date 2015-08-28

URL http://hdl.handle.net/2433/214532

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© 2015 Wolsan et al. This is an open access article distributedunder the terms of the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproductionin any medium, provided the original author and source arecredited

Type Journal Article

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Kyoto University

RESEARCH ARTICLE

Tooth Size Variation in Pinniped DentitionsMieczyslawWolsan1,2*, Satoshi Suzuki1¤a, Masakazu Asahara3¤b, Masaharu Motokawa1

1 The Kyoto University Museum, Kyoto University, Kyoto, Japan, 2 Museum and Institute of Zoology, PolishAcademy of Sciences, Warsaw, Poland, 3 Department of Zoology, Graduate School of Science, KyotoUniversity, Kyoto, Japan

¤a Current Address: Fukui City Museum of Natural History, Fukui, Japan¤b Current Address: Primate Research Institute, Kyoto University, Inuyama, Japan* [email protected]

AbstractIt is contentious whether size variation among mammalian teeth is heterogeneous or homo-

geneous, whether the coefficient of variation is reliable, and whether the standard deviation

of log-transformed data and the residual of standard deviation on mean variable size are

useful replacements for the coefficient of variation. Most studies of tooth size variation have

been on mammals with complex-crowned teeth, with relatively little attention paid to taxa

with simple-crowned teeth, such as Pinnipedia. To fill this gap in knowledge and to resolve

the existing controversies, we explored the variation of linear size variables (length and

width) for all teeth from complete permanent dentitions of four pinniped species, two pho-

cids (Histriophoca fasciata, Phoca largha) and two otariids (Callorhinus ursinus, Eumetopiasjubatus). Size variation among these teeth was mostly heterogeneous both along the tooth-

row and among species. The incisors, canines, and mesial and distal postcanines were

often relatively highly variable. The levels of overall dental size variation ranged from rela-

tively low as in land carnivorans (Phoca largha and both otariids) to high (Histriophoca fas-ciata). Sexual size dimorphism varied among teeth and among species, with teeth being, on

average, larger in males than in females. This dimorphism was more pronounced, and the

canines were larger and more dimorphic relative to other teeth in the otariids than in the pho-

cids. The coefficient of variation quantified variation reliably in most cases. The standard

deviation of log-transformed data was redundant with the coefficient of variation. The resid-

ual of standard deviation on mean variable size was inaccurate when size variation was

considerably heterogeneous among the compared variables, and was incomparable

between species and between sexes. The existing hypotheses invoking developmental

fields, occlusal complexity, and the relative timing of tooth formation and sexually dimorphic

hormonal activity do not adequately explain the differential size variation along the pinniped

toothrow.

PLOS ONE | DOI:10.1371/journal.pone.0137100 August 28, 2015 1 / 28

OPEN ACCESS

Citation:Wolsan M, Suzuki S, Asahara M,Motokawa M (2015) Tooth Size Variation in PinnipedDentitions. PLoS ONE 10(8): e0137100. doi:10.1371/journal.pone.0137100

Editor: Matthew C. Mihlbachler, NYIT College ofOsteopathic Medicine, UNITED STATES

Received: February 2, 2015

Accepted: August 12, 2015

Published: August 28, 2015

Copyright: © 2015 Wolsan et al. This is an openaccess article distributed under the terms of theCreative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in anymedium, provided the original author and source arecredited.

Data Availability Statement: All relevant data arewithin the paper.

Funding: Partial support for this work came from theNational Science Centre (www.ncn.gov.pl) throughgrant 2012/05/B/NZ8/02687 to MW. MA wassupported during part of this study by a JapanSociety for the Promotion of Science (www.jsps.go.jp)research fellowship for young scientists (11J01149).The funders had no role in study design, datacollection and analysis, decision to publish, orpreparation of the manuscript.

Competing Interests: The authors have declaredthat no competing interests exist.

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IntroductionVariation is a prerequisite for evolution by natural selection. Therefore, variation has been thefocus of considerable biological research for over 150 years [1–3]. No characterization of ataxon, population, organism, or organ can be complete without characterizing its variation.

Dentition is of fundamental importance for the study of mammalian evolution. This isbecause teeth are highly informative of a mammal’s taxonomic identity, ecological adaptation,and phylogenetic relationships, and because they are chiefly inorganic, which makes themdurable and relatively abundant in the fossil record [4, 5]. The size of a tooth crown is fixed bythe cessation of enamel apposition before tooth eruption, offering a correlate to body size [6–9], which in turn correlates with many aspects of an animal’s life history and ecology [10, 11].

A common index of variation is CV, which is the ratio of SD to mean (these and other statis-tical abbreviations used in the paper are explained in Table 1). Because ME tends to uniformlycontribute to SD, CV is usually negatively correlated with mean variable size and may becomeartificially high if the ME of a variable is high and the variable is small [12]. To counteract thisbias in CV, two alternative measures of variation (SDL and RSD) were proposed [12]. SDL andRSD have been used in several studies [12–15], but the usefulness of these indices and the reli-ability of CV, though discussed [12–17], have remained largely unexplored.

An array of studies have documented (using CV) patterns of variation in tooth size withinmammalian dentitions, with certain teeth being consistently more or less variable than others(e.g., [13, 14, 18–28]). These patterns have been explained in terms of the relative position ofteeth in a developmental [29] (morphogenetic [30] or growth [31]) field [18, 19, 24, 32], the rel-ative occlusal complexity of tooth crowns [13, 15, 20, 21], or the relative timing of tooth forma-tion and sexually dimorphic hormonal activity [12–15, 18]. The hypothesis invoking relativetooth position in a developmental field assumes that the level of variation in the size of a toothdepends on the position of that tooth in an incisor, canine, or postcanine field and that teeth inthe center of such a developmental field are less variable than those at the periphery of thatfield [18, 19]. The hypothesis invoking relative tooth occlusal complexity postulates that thelevel of size variation in teeth is inversely proportional to their occlusal complexity [20].

Table 1. Explanation of Statistical Abbreviations and Symbols.

Abbreviation orsymbol

Name and/or definition

CV Coefficient of variation, or the ratio of the standard deviation of a variable to thearithmetic mean of that variable, multiplied by 100

M/F Sexual size dimorphism index, or the ratio of the arithmetic mean of a variable inmales to the arithmetic mean of that variable in females

ME Measurement error, or [s2ind/(s2ind + s2pop)] × 100, where s2ind is the variance of

the repeated measurements of a variable in a single individual, and s2pop is thevariance of the measurements of that variable among all individuals in the sample[12]

mean Arithmetic mean

n Sample size

P Probability of wrongly rejecting the null hypothesis of no difference or relationship

r Pearson’s product moment correlation coefficient

rs Spearman’s rank correlation coefficient

RSD Residual of the standard deviation of a variable regressed on the arithmetic meanof that variable

SD Standard deviation

SDL Standard deviation of log-transformed data

doi:10.1371/journal.pone.0137100.t001

Pinniped Tooth Size Variation


Finally, the hypothesis invoking the relative timing of tooth formation and sexually dimorphichormonal activity proposes that teeth forming before the onset of sex-linked differentiation inhormonal balance are less variable than those forming during sexually differentiated growthand that the latter teeth show progressively higher variation indices when males and femalesare pooled [18].

Polly [12] argued that the observed patterns of variation were the effect of size-related biasin CV and that size variation among mammalian teeth is indeed relatively homogeneous bothwithin and among species. The generality of this conclusion was undermined by subsequentstudies [14–17], which showed that the patterns of tooth size variation seen in the dentitions ofvarious land carnivorans were not entirely generated by bias in CV.

Variation in tooth size has been studied in various mammalian clades, mainly in primates(e.g., [19, 20, 22, 23, 26–28, 33]) and canids (e.g., [12–14, 16, 21, 24, 34–39]). Most studies havebeen on taxa with complex-crowned teeth, which prevail among mammals, with relatively littleattention paid to taxa with simple-crowned teeth, such as Pinnipedia, a clade of aquatic (mostlymarine) carnivorans (Fig 1). The only study of tooth size variation using a large sample from apinniped species to date has been that of Miller et al. [40], who investigated the ringed seal’s(Pusa hispida) third lower premolar and the harp seal’s (Pagophilus groenlandicus) lower post-canines. These authors found that CVs for size variables of these teeth were higher than thosein the compared land carnivorans and therefore hypothesized that the postcanines of

Fig 1. Vestibular Profiles of Upper (Left) and Lower (Right) Pinniped Permanent Dentitions. A, B, northern fur seal (Callorhinus ursinus), female, KUZM10142 (KUZ, Kyoto University Museum); C, D, Steller sea lion (Eumetopias jubatus), female, KUZ M9290; E, F, ribbon seal (Histriophoca fasciata), male,KUZ M9575; G, H, spotted seal (Phoca largha), female, KUZ M9465, reversed mirror image. Scale bars equal 1 cm.

doi:10.1371/journal.pone.0137100.g001



pinnipeds are more variable in size than those of land carnivorans due to evolutionary simplifi-cation of morphology via selective release.

The purpose of this study was fourfold: (1) to evaluate the reliability and usefulness of CV,SDL, and RSD; (2) to describe and compare the variation of tooth size within and among spe-cies of Pinnipedia representing its two major extant clades, Otariidae and Phocidae; (3) to com-pare the variation of tooth size between pinnipeds and land carnivorans; and (4) to testhypotheses related to tooth size variation. Specifically, we test the following hypotheses: (1)that CV is not a reliable measure of variation and that SDL and RSD are more reliable [12]; (2)that size variation among mammalian teeth is relatively homogeneous both within and amongspecies except highly variable canines in some species [12]; (3) that the postcanines of pinni-peds are more variable in size than those of land carnivorans due to evolutionary simplificationof morphology [40]; (4) that the level of variation in the size of a tooth depends on the positionof that tooth in an incisor, canine, or postcanine developmental field, with teeth in the centerof that field being less variable than those at the periphery [18, 19]; (5) that the level of size vari-ation in teeth is inversely proportional to their occlusal complexity [20]; and (6) that teethforming before the onset of sex-linked differentiation in hormonal balance are less variablethan those forming during sexually differentiated growth, with the latter teeth showing pro-gressively higher variation indices when males and females are pooled [18].

Materials and MethodsMeasurements were collected from permanent dentitions in skeletonized specimens of fourspecies representing two families of Pinnipedia from the collections of five institutions (Fig 1,Tables 2 and 3). According to the collection records, these specimens derived from wild ani-mals on and around the Japanese Islands. For each specimen, two linear size variables (lengthand width; Table 4) were measured on all teeth of one body side, left or right, depending on thestate of preservation. All measurements were taken with digital calipers to the nearest 0.01mm. ME was assessed by measuring variables 10 times for one randomly selected specimen.Size variation was quantified using three indices: CV, SDL, and RSD. Sexual size dimorphismwas evaluated with M/F [41]. Data on the complete sequence of tooth eruption were takenfrom the relevant literature (these data were available only for Callorhinus ursinus). Statisticalanalyses were performed in R versions 2.13.2 and 3.0.2 [42].

Results

Tooth sizeMean variable size was 2.23–12.23 mm in Callorhinus ursinus (Fig 2A, Table 6), 3.33–23.64mm in Eumetopias jubatus (Fig 3A, Table 7), 1.07–5.67 mm inHistriophoca fasciata (Fig 4A,Table 8), and 1.87–9.35 mm in Phoca largha (Fig 5A, Table 9). All teeth were, on average, larg-est in E. jubatus, smallest inH. fasciata, and intermediate in size in C. ursinus and P. largha(Figs 6A and 7A).

In all species, I1 was smaller than I2, I2 was smaller than I3, and I2 was smaller than I3. Theincisors had the smallest mean mesiodistal length in all species except I3 in male E. jubatus andI3 in male C. ursinus. I1 in all species except C. ursinus, I2 in all species except C. ursinus andmale E. jubatus, and both lower incisors in all species had the smallest mean vestibulolingualwidth (Figs 2A, 3A, 4A and 5A).

The canines were the largest teeth in both the upper and lower dentitions in all species (Fig1). The canines had the greatest mean vestibulolingual width in all species and the greatestmean mesiodistal length in C. ursinus and E. jubatus; C1 also had the greatest mean length inmale H. fasciata. C1 in female and C1 in female and male H. fasciata as well as both canines in



both sexes of P. largha had a smaller mean length than one or more postcanines in the tooth-row (Figs 2A, 3A, 4A and 5A). The postcanines that significantly (P� 0.05, Welch’s t-test)

Table 3. Institutional Abbreviations.

Abbreviation Name

HUM Hokkaido University Museum, Hokkaido University, Sapporo, Japan

HUNHM Botanic Garden, Hokkaido University, Sapporo, Japan

KUZ Kyoto University Museum, Kyoto University, Kyoto, Japan

NSMT National Museum of Nature and Science, Tokyo, Japan

TUA Laboratory of Aquatic Management, Department of Aqua Bioscience and Industry, Facultyof Bioindustry, Tokyo University of Agriculture, Abashiri, Japan


Table 2. Measured Specimens.

Family Species Males Females

Otariidae Callorhinus ursinus(Linnaeus, 1758) [43]

HUNHM 9893, 11560, 13349; KUZ M10017, M10019,M10023, M10027, M10031, M10033, M10034,M10043, M10051, M10067–M10069, M10092–M10095, M10098, M10099, M10101–M10103,M10106–M10110, M10113, M10116, M10120,M10121, M10124, M10126, M10141, M10279,M10281, M10372; NSMT KK70, KK162, M1994,M1996

KUZ M10018, M10020, M10021, M10024, M10029,M10035, M10038, M10040, M10041, M10044–M10046,M10048–M10050, M10053, M10055, M10056,M10058–M10062, M10064, M10065, M10081, M10082,M10085, M10087, M10089, M10090, M10114, M10115,M10119, M10123, M10125, M10127–M10129, M10131,M10132, M10135, M10137, M10138, M10140, M10142,M10144, M10147–M10149, M10151, M10154, M10155,M10157; NSMT KK8, KK10, KK22, KK151, M1995

Eumetopias jubatus(Schreber, 1776) [44]

HUM 1, 3, 4, 6, 13, 16, 21, 22, 31; KUZ M9286, M9436,M9438, M9581, M9586, M9588, M9590, M9594,M9985, M9987–M9991, M9993, M9994, M10001,M10004–M10006; NSMT KK42, KK122

HUNHM 13313, 13351; KUZ M9290, M9291, M9295,M9297, M9309, M9311, M9437, M9440–M9442,M9968; NSMT KK55, KK62, KK67, KK125, KK131,KK135, KK139, KK146, KK154, KK156, KK158,M17123, M24719, M24723, M24724, N113, PO136

Phocidae Histriophoca fasciata(Zimmermann, 1783)[45]

HUNHM 17216, 17217, 17246, 17249; KUZ M9397,M9398, M9401, M9407, M9409, M9425, M9454,M9460, M9466, M9493, M9559, M9572, M9575,M9577, M9605, M9608, M9619, M9639, M9640,M9645, M9647, M9657, M9659, M9665, M9671,M9680, M9682, M9685, M9688, M9711, M9720,M9724, M9770, M9771, M9801, M9808, M9813,M9823, M9856, M9858, M9861, M9875, M9876,M9884, M9976, M10370; TUA 349, NK502, P265,P274, P275, P291, P297, P300, RK501, RK502,RK505, RK507

HUM 10, 44; HUNHM 17222, 47748, 47749; KUZM9312, M9314, M9325, M9334, M9338, M9341,M9342, M9411, M9427, M9453, M9469, M9473,M9482, M9483, M9500, M9501, M9550, M9556,M9569, M9571, M9574, M9607, M9617, M9621,M9646, M9653, M9654, M9660, M9663, M9667,M9668, M9670, M9674, M9677–M9679, M9684,M9687, M9691, M9692, M9708, M9712–M9715,M9718, M9755, M9756, M9763, M9766, M9768,M9769, M9772, M9809, M9811, M9826–M9829,M9831, M9832, M9835, M9836, M9857, M9859,M9863, M9870–M9872, M9877–M9879; TUA 348b,P269, P279, P294, P295, P301, RK509, RK511, RK512

Phoca largha Pallas,1811 [46]

HUNHM 13325, 13326; KUZ M9277, M9279, M9336,M9413, M9415, M9457, M9533, M9548, M9610,M9623, M9741, M9745, M9851, M9902, M10342;NSMT M24771, M29787; TUA AbG701, BG902,BG905, EG5101, G18, G21, G29, HAG604, HAG607,HAG608, HAG612, NG301, NG304, NG305, NG505,NG506, NG508–NG510, NoG911, ReG909, ReG911,ReG1004, ReG1007, ReG1008, ReG1010, RG502–RG506, RG508–RG510, RG512, RG513, RG516,RG517, RG520, RG522, RG526, RG530, RG708,RG710, RG804, RG805, RG913, RG918–RG920,RG925, YG401–YG404, YG502, YG503, YG601,YG701, YG704, YG906

KUZ M9264, M9348, M9465, M9499, M9502, M9505,M9507, M9537, M9749, M9784, M9868; NSMTM28385; TUA AbG702, AbG703, AbG902, AG2,BG903, BG904, BG906, G2, G4, G23, HAG601,HAG602, HAG605, HAG606, HAG609, HAG611,NG302, NG303, NG306, NG504, ReG908, ReG912,ReG1001, ReG1002, ReG1006, ReG1009, ReG1011,RG523–RG525, RG528, RG529, RG533, RG534,RG712, RG801, RG802, RG901, RG903, RG922,RK510, YG405, YG501, YG507, YG602, YG603,YG702, YG703

Institutional abbreviations are explained in Table 3.




Table 4. Tooth Size Variables.

Abbreviation Name Definition

LC1 Length ofC1

Longest linear mesiodistal distance on the crown of C1

LC1 Length ofC1

Longest linear mesiodistal distance on the crown of C1

LI1 Length of I1 Longest linear mesiodistal distance on the crown of I1

LI2 Length of I2 Longest linear mesiodistal distance on the crown of I2

LI2 Length of I2 Longest linear mesiodistal distance on the crown of I2LI3 Length of I3 Longest linear mesiodistal distance on the crown of I3

LI3 Length of I3 Longest linear mesiodistal distance on the crown of I3LM1 Length of

M1Longest linear mesiodistal distance on the crown of M1

LM1 Length ofM1

Longest linear mesiodistal distance on the crown of M1

LM2 Length ofM2

Longest linear mesiodistal distance on the crown of M2

LP1 Length ofP1

Longest linear mesiodistal distance on the crown of P1

LP1 Length ofP1


LP2 Length ofP2


LP2 Length ofP2


LP3 Length ofP3


LP3 Length ofP3


LP4 Length ofP4


LP4 Length ofP4


WC1 Width of C1 Longest linear vestibulolingual distance on the crown of C1 perpendicular toLC1

WC1 Width of C1 Longest linear vestibulolingual distance on the crown of C1 perpendicular toLC1

WI1 Width of I1 Longest linear vestibulolingual distance on the crown of I1 perpendicular toLI1





WM1 Width of M1 Longest linear vestibulolingual distance on the crown of M1 perpendicular toLM1



WP1 Width of P1 Longest linear vestibulolingual distance on the crown of P1 perpendicular toLP1

(Continued)



exceeded the canine of the toothrow in mean length were P3, P4, and M1 in male and female H.fasciata; P3, P2, P3, P4, and M1 in male and female P. largha; and P4 in female P. largha.

The postcanines were largely of similar size within the toothrow (Fig 1) and partly varied insequence according to size within species. In C. ursinus, M1 was the mesiodistally longestupper postcanine in most specimens, M2 was the shortest in most specimens, and the upperpremolars were vestibulolingually broader than the upper molars (with M1 mostly broader

Table 4. (Continued)

Abbreviation Name Definition








Tooth symbols are explained in Table 5.


Table 5. Explanation of Tooth Symbols.

Symbol Name

C1 Upper canine

C1 Lower canine

I1 First upper incisor

I1 First lower incisor

I2 Second upper incisor

I2 Second lower incisor

I3 Third upper incisor

I3 Third lower incisor

M1 First upper molar

M1 First lower molar

M2 Second upper molar

M2 Second lower molar

M3 Third lower molar

P1 First upper premolar

P1 First lower premolar

P2 Second upper premolar

P2 Second lower premolar

P3 Third upper premolar

P3 Third lower premolar

P4 Fourth upper premolar

P4 Fourth lower premolar




than M2). M1 was in most cases the longest lower postcanine, P1 was the shortest and in mostcases the narrowest, P2 was the second shortest, and P4 was in most cases the broadest (Fig2A).

In E. jubatus, P2 was the longest upper postcanine in most specimens, whereas P1 or, morerarely, M1 was the shortest. P2 and P3 were broader than other upper postcanines. M1 was thenarrowest upper postcanine. P3 was the longest and broadest lower postcanine. P1 and M1

were shorter than other lower postcanines (P1 was in most cases shorter than M1). M1 was inmost cases the narrowest lower postcanine, and P1 was in most cases the second narrowest (Fig3A).

In H. fasciata, P3 and P4 were longer and broader than other upper postcanines in mostspecimens. P1 was in most cases the shortest upper postcanine, and M1 was in most cases thenarrowest. P3 and P4 were longer and broader than other lower postcanines in most specimens.

Fig 2. Arithmetic Mean and Variation Indices for Tooth Lengths andWidths Varied along the Toothrow and between Sexes inCallorhinus ursinus.A, arithmetic mean (mean); B, coefficient of variation (CV); C, standard deviation of log-transformed data (SDL); D, residual of standard deviation onarithmetic mean (RSD). Data from Table 6. Abbreviations for tooth lengths and widths are explained in Table 4.




Table 6. Statistics for Tooth Lengths andWidths inCallorhinus ursinus.

Variable Males, n = 43 Females, n = 59 M/F

Range mean SD ME CV SDL RSD Range mean SD ME CV SDL RSD

Lengths of upper teeth

LI1 2.09–2.71 2.42** 0.15 0.33 6.1 0.027 -0.016 1.88–2.52 2.23 0.14 0.24 6.2 0.027 -0.046 1.08

LI2 2.33–3.06 2.69** 0.16 0.28 6.1 0.027 -0.020 2.18–2.80 2.53 0.15 1.83 6.1 0.027 -0.046 1.07

LI3 3.86–5.62 4.61** 0.45 3.75 9.8 0.042 0.116 2.86–4.64 3.62 0.35 1.03 9.7 0.042 0.085 1.27

LC1 10.15–15.51 12.06** 0.97 0.13 8.0 0.034 0.057 6.87–9.29 7.84 0.64 0.24 8.2 0.035 0.127 1.54

LP1 5.35–7.11 6.16** 0.38 0.21 6.2 0.027 -0.074 4.86–6.19 5.55 0.27 0.18 4.9 0.021 -0.104 1.11

LP2 5.38–6.83 6.23** 0.34 0.05 5.4 0.024 -0.123 5.02–6.47 5.60 0.30 0.13 5.4 0.023 -0.078 1.11

LP3 5.35–7.07 6.24** 0.38 0.26 6.1 0.026 -0.083 5.06–6.54 5.63 0.33 0.06 5.8 0.025 -0.055 1.11

LP4 5.25–7.14 6.38** 0.41 0.05 6.4 0.028 -0.062 5.08–6.84 5.85 0.40 0.12 6.8 0.029 0.001 1.09

LM1 5.70–7.56 6.70** 0.38 0.03 5.6 0.025 -0.119 5.36–7.38 6.29 0.46 0.16 7.3 0.032 0.038 1.07

LM2 2.89–6.45 5.31** 0.78 0.00 14.7 0.074 0.394 2.73–5.85 4.72 0.68 0.02 14.4 0.071 0.351 1.13

Widths of upper teeth

WI1 3.64–5.19 4.37** 0.35 0.11 7.9 0.035 0.031 3.25–4.48 3.78 0.26 0.78 6.9 0.029 -0.014 1.16

WI2 3.94–5.48 4.69** 0.34 0.04 7.2 0.031 -0.002 3.50–4.79 4.10 0.27 0.37 6.5 0.028 -0.028 1.14

WI3 5.51–7.95 6.73** 0.55 0.27 8.2 0.036 0.053 4.28–6.08 5.20 0.46 0.99 8.9 0.040 0.107 1.30

WC1 7.57–11.38 9.18** 0.81 0.72 8.9 0.039 0.124 4.69–6.89 5.82 0.47 0.06 8.1 0.035 0.075 1.58

WP1 4.05–5.45 4.76** 0.36 0.19 7.6 0.033 0.018 3.71–5.06 4.33 0.29 0.90 6.7 0.029 -0.015 1.10

WP2 3.95–5.43 4.67** 0.35 0.07 7.6 0.033 0.015 3.68–4.86 4.19 0.26 0.67 6.3 0.027 -0.035 1.11

WP3 4.04–5.41 4.62** 0.31 2.49 6.7 0.029 -0.024 3.64–4.80 4.22 0.26 1.69 6.3 0.027 -0.035 1.09

WP4 3.93–5.09 4.56** 0.28 0.11 6.2 0.027 -0.049 3.68–4.81 4.20 0.27 3.05 6.4 0.028 -0.029 1.09

WM1 2.88–4.18 3.55* 0.24 0.27 6.8 0.030 -0.009 2.82–4.01 3.39 0.28 0.25 8.4 0.037 0.033 1.05

WM2 2.42–3.93 3.29** 0.32 0.29 9.7 0.044 0.088 2.28–3.54 2.97 0.28 1.10 9.3 0.041 0.051 1.11

Lengths of lower teeth

LI2 2.63–3.51 3.17** 0.19 0.39 6.0* 0.026 -0.033 2.41–4.20 2.99 0.27 0.12 9.0 0.037 0.042 1.06

LI3 4.71–6.93 5.73** 0.50 1.68 8.7* 0.038 0.078 4.35–5.89 4.94 0.32 1.53 6.5 0.028 -0.021 1.16

LC1 10.10–15.54 12.23** 0.94 0.22 7.7 0.032 0.012 6.08–8.56 6.95 0.52 1.69 7.5 0.032 0.058 1.76

LP1 4.49–6.35 5.50** 0.35 0.93 6.5* 0.028 -0.048 4.68–5.57 5.08 0.24 0.91 4.8 0.021 -0.109 1.08

LP2 5.42–6.86 6.17** 0.30 2.08 4.9 0.021 -0.153 5.00–6.34 5.55 0.29 0.07 5.2 0.022 -0.090 1.11

LP3 5.87–7.46 6.75** 0.37 1.61 5.5 0.024 -0.127 5.39–6.69 6.02 0.31 0.07 5.1 0.022 -0.100 1.12

LP4 6.03–7.62 6.83** 0.38 0.27 5.6 0.024 -0.125 5.32–7.13 6.15 0.34 0.11 5.5 0.024 -0.078 1.11

LM1 6.20–8.33 7.24** 0.44 0.24 6.1 0.026 -0.098 5.89–7.68 6.65 0.36 0.04 5.4 0.023 -0.083 1.09

Widths of lower teeth

WI2 2.78–3.84 3.19** 0.26 0.47 8.0 0.034 0.032 2.23–3.29 2.73 0.22 0.11 8.0 0.035 0.006 1.17

WI3 2.68–4.53 3.46** 0.37 0.53 10.7 0.046 0.125 2.25–3.17 2.77 0.23 2.17 8.3 0.037 0.016 1.25

WC1 5.68–8.99 7.44** 0.73 0.45 9.8 0.043 0.177 4.04–5.67 4.78 0.38 1.58 8.0 0.034 0.049 1.56

WP1 3.37–4.43 3.92** 0.26 1.30 6.7 0.029 -0.017 2.90–4.33 3.64 0.27 1.27 7.5 0.033 0.007 1.08

WP2 3.55–4.99 4.30** 0.29 0.83 6.7 0.029 -0.022 3.08–4.42 3.80 0.28 0.26 7.4 0.033 0.006 1.13

WP3 4.03–5.30 4.58** 0.28 1.73 6.1 0.026 -0.053 3.39–4.69 4.03 0.26 0.45 6.5 0.028 -0.027 1.14

WP4 4.20–5.43 4.70** 0.29 0.11 6.1 0.026 -0.053 3.39–4.67 4.17 0.26 1.25 6.3 0.028 -0.033 1.13

WM1 3.49–4.81 4.12** 0.29 0.24 7.0 0.030 -0.008 3.32–4.38 3.81 0.25 0.71 6.5 0.028 -0.026 1.08

Range, mean, SD, and RSD are given in millimeters, SDL is in log millimeters, ME and CV are in per cent. Asterisks indicate the means and CVs of males

that differ significantly (*P � 0.05, **P � 0.001) from those of females according to Welch’s t-test (means) or Z-test (CVs) results. Statistical abbreviations

and symbols are explained in Table 1. Abbreviations for tooth lengths and widths are expanded in Table 4.




P1 was the shortest and in most cases the narrowest lower postcanine, P2 was in most cases thesecond shortest, and M1 was in most cases the second narrowest (Fig 4A).

In P. largha, P3 was the longest upper postcanine in most specimens, P4 was the broadest inmost specimens, and P1 was the shortest and in most cases the narrowest. P3 and M1 were lon-ger than other lower postcanines in most specimens (M1 was in most cases longer than P3). P3was also in most cases the broadest lower postcanine, and P1 was both the shortest and the nar-rowest (Fig 5A).

Measurement errorMEs ranged 0.00–3.75% in C. ursinus (Table 6), 0.01–4.69% in E. jubatus (Table 7), 0.01–1.34% in H. fasciata (Table 8), and 0.01–2.53% in P. largha (Table 9). ME and mean variablesize were negatively correlated in all species, but this correlation was significant only inH. fas-ciata and female P. largha (Table 10).

Fig 3. Arithmetic Mean and Variation Indices for Tooth Lengths andWidths Varied along the Toothrow and between Sexes in Eumetopias jubatus.A, arithmetic mean (mean); B, coefficient of variation (CV); C, standard deviation of log-transformed data (SDL); D, residual of standard deviation onarithmetic mean (RSD). Data from Table 7. Abbreviations for tooth lengths and widths are explained in Table 4.




Table 7. Statistics for Tooth Lengths andWidths in Eumetopias jubatus.




LI1 3.43–4.19 3.79** 0.21 0.97 5.5 0.024 0.019 3.05–3.62 3.33 0.15 0.26 4.4 0.019 -0.076 1.14

LI2 3.85–5.50 4.70** 0.38 0.09 8.2 0.036 0.127 3.59–4.71 4.14 0.29 0.19 7.0 0.030 0.028 1.13

LI3 9.91–13.14 11.70** 0.69 0.51 5.9 0.026 -0.093 7.35–9.92 8.40 0.69 1.32 8.2 0.035 0.224 1.39

LC1 18.83–27.26 21.84** 1.76 0.08 8.1 0.034 0.217 10.94–14.72 13.25 0.78 0.16 5.9 0.026 0.086 1.65

LP1 9.26–12.66 11.03** 0.67 0.08 6.1 0.027 -0.058 8.47–10.58 9.69 0.49 0.99 5.0 0.022 -0.036 1.14

LP2 11.98–15.16 13.34** 0.68 0.41 5.1 0.022 -0.227 10.66–12.62 11.53 0.46 1.53 4.0 0.017 -0.149 1.16

LP3 12.24–14.49 12.99** 0.60 0.37 4.6 0.020 -0.276 10.20–12.64 11.29 0.52 0.52 4.6 0.020 -0.080 1.15

LP4 11.63–14.20 12.68** 0.63 4.69 5.0 0.021 -0.229 10.15–12.44 11.25 0.53 0.38 4.7 0.020 -0.068 1.13

LM1 7.30–13.55 11.11* 1.12 0.11 10.0* 0.047 0.377 9.54–12.05 10.36 0.60 0.04 5.8 0.025 0.045 1.07


WI1 5.40–6.77 6.06** 0.38 1.05 6.2 0.027 0.016 4.54–5.53 5.02 0.27 0.52 5.3 0.023 -0.034 1.21

WI2 6.34–8.54 7.47** 0.59 0.16 8.0* 0.035 0.128 5.55–6.74 6.04 0.29 0.70 4.8 0.021 -0.059 1.24

WI3 12.48–16.26 14.26** 0.92 0.08 6.4 0.028 -0.060 9.52–12.18 10.56 0.75 0.46 7.1 0.030 0.181 1.35

WC1 16.06–22.89 18.82** 1.36 0.02 7.2 0.031 0.045 10.09–12.01 10.98 0.56 0.15 5.1 0.022 -0.028 1.71

WP1 7.18–9.68 8.68** 0.60 0.38 6.9 0.030 0.039 6.58–8.42 7.67 0.39 0.25 5.1 0.022 -0.038 1.13

WP2 8.42–11.10 10.06** 0.64 0.20 6.3 0.028 -0.024 8.17–9.65 8.86 0.42 0.33 4.8 0.021 -0.061 1.14

WP3 9.07–11.49 10.16** 0.58 0.21 5.7 0.025 -0.086 7.74–9.77 8.90 0.45 0.01 5.1 0.023 -0.033 1.14

WP4 7.79–10.48 8.74** 0.62 0.30 7.1 0.030 0.064 6.64–8.78 7.79 0.47 0.59 6.0 0.026 0.033 1.12

WM1 6.04–7.67 6.80** 0.38 0.30 5.7 0.025 -0.030 5.32–6.94 6.10 0.42 0.79 6.9 0.030 0.066 1.12


LI2 4.22–6.04 5.17** 0.37 0.34 7.2 0.031 0.078 3.99–5.08 4.62 0.26 2.75 5.7 0.025 -0.018 1.12

LI3 8.25–10.76 9.08** 0.57 0.12 6.2 0.027 -0.021 7.17–8.74 8.07 0.47 0.81 5.9 0.026 0.025 1.13

LC1 20.06–28.98 23.64** 1.89 0.07 8.0* 0.034 0.210 11.71–14.69 12.98 0.67 0.33 5.2 0.022 -0.008 1.82

LP1 8.92–11.57 10.18** 0.61 0.19 6.0 0.026 -0.059 6.03–9.64 8.86 0.62 0.14 7.0 0.035 0.139 1.15

LP2 11.41–13.03 12.24** 0.49 0.22 4.0 0.017 -0.333 10.09–11.76 10.89 0.45 0.04 4.2 0.018 -0.128 1.12

LP3 12.98–15.53 14.15** 0.68 0.13 4.8 0.021 -0.292 11.14–13.30 12.36 0.54 0.25 4.3 0.019 -0.113 1.15

LP4 11.58–14.60 12.97** 0.84 0.03 6.4 0.028 -0.043 9.14–12.90 11.41 0.71 0.08 6.2 0.028 0.104 1.14

LM1 8.84–11.55 10.45** 0.71 0.05 6.8 0.030 0.024 7.81–10.96 9.49 0.71 0.15 7.5 0.033 0.199 1.10


WI2 5.27–6.81 5.94** 0.40 0.37 6.7 0.029 0.050 4.20–5.46 4.96 0.30 0.42 6.1 0.027 0.003 1.20

WI3 5.82–8.76 6.67** 0.56 0.22 8.4 0.035 0.156 4.74–6.34 5.41 0.33 1.27 6.1 0.026 0.012 1.23

WC1 13.53–18.93 16.11** 1.29 0.18 8.0** 0.035 0.175 8.18–9.63 8.84 0.35 1.97 4.0 0.017 -0.134 1.82

WP1 6.75–8.70 7.68** 0.52 0.17 6.8 0.030 0.039 5.76–7.40 6.64 0.39 0.05 5.8 0.026 0.007 1.16

WP2 7.13–9.30 8.32** 0.49 0.85 5.9 0.026 -0.036 6.45–8.00 7.18 0.39 0.06 5.5 0.024 -0.013 1.16

WP3 8.41–10.60 9.43** 0.59 0.68 6.3* 0.027 -0.023 7.46–8.88 8.03 0.34 0.07 4.3 0.018 -0.101 1.18

WP4 7.44–10.10 8.77** 0.65 0.34 7.4 0.032 0.086 6.25–8.37 7.54 0.46 0.11 6.1 0.027 0.035 1.16

WM1 5.98–7.95 6.85** 0.46 0.16 6.8 0.029 0.045 5.40–6.66 6.02 0.34 0.71 5.7 0.025 -0.009 1.14







Variation indicesCVs and SDLs were in most cases highest in H. fasciata, in most cases lowest in E. jubatus, andin most cases intermediate in C. ursinus and P. largha (Figs 6B, 6C, 7B and 7C). Both the high-est and lowest RSDs were most frequent in E. jubatus (Figs 6D and 7D). H. fasciata had thewidest range of CVs, C. ursinus had the widest range of SDLs, and E. jubatus had the widestrange of RSDs; P. largha showed the narrowest range for all of these indices. Specifically, CVs,SDLs, and RSDs, respectively, ranged 4.8–14.7%, 0.021–0.074 log mm, and -0.153–0.394 mmin C. ursinus (Fig 2B–2D, Table 6); 4.0–10.0%, 0.017–0.047 log mm, and -0.333–0.377 mm inE. jubatus (Fig 3B–3D, Table 7); 7.3–18.5%, 0.032–0.080 log mm, and -0.104–0.187 mm inH.fasciata (Fig 4B–4D, Table 8); and 5.4–9.9%, 0.024–0.044 log mm, and -0.062–0.115 mm in P.largha (Fig 5B–5D, Table 9). As expected, CVs and SDLs were in most cases higher whenmales and females were pooled (for C. ursinus, compare Table 6 and Fig 8).

Fig 4. Arithmetic Mean and Variation Indices for Tooth Lengths andWidths Varied along the Toothrow and between Sexes inHistriophocafasciata. A, arithmetic mean (mean); B, coefficient of variation (CV); C, standard deviation of log-transformed data (SDL); D, residual of standard deviationon arithmetic mean (RSD). Data from Table 8. Abbreviations for tooth lengths and widths are explained in Table 4.




When the variation indices were compared among the classes of teeth within the toothrow,the indices for incisors were largely relatively high. The incisor indices varied from the lowest(CV, SDL, and RSD in P. largha, and RSD inH. fasciata) to the highest (CV, SDL, and RSD in

Table 8. Statistics for Tooth Lengths andWidths inHistriophoca fasciata.




LI1 1.27–2.28 1.80* 0.21 0.39 11.9 0.055 -0.033 1.12–2.27 1.71 0.19 0.09 10.9 0.049 -0.025 1.05

LI2 1.50–2.71 2.04 0.24 0.20 12.0 0.052 -0.022 1.42–2.80 1.98 0.23 0.26 11.5 0.050 -0.006 1.03

LI3 2.23–3.82 2.97 0.34 0.12 11.5* 0.050 -0.000 2.24–3.50 2.89 0.26 0.21 9.0 0.040 -0.045 1.03

LC1 4.54–6.62 5.52* 0.52 0.09 9.4 0.041 -0.030 4.18–6.39 5.29 0.40 0.12 7.6 0.033 -0.096 1.04

LP1 3.17–5.34 4.08 0.45 0.01 11.0 0.048 0.019 2.77–5.11 3.95 0.40 0.38 10.2 0.045 0.012 1.03

LP2 3.67–6.12 4.73 0.56 0.04 11.9 0.052 0.080 3.33–5.78 4.57 0.45 0.28 9.8 0.043 0.007 1.04

LP3 4.09–6.83 5.33 0.51 0.08 9.5 0.041 -0.026 3.76–6.33 5.30 0.52 0.09 9.9 0.044 0.025 1.01

LP4 4.19–6.94 5.24 0.52 0.02 10.0 0.043 -0.002 3.75–6.40 5.19 0.50 0.27 9.5 0.043 0.005 1.01

LM1 3.76–5.85 4.69* 0.46 0.07 9.8 0.043 -0.020 3.19–5.71 4.51 0.53 0.02 11.9 0.053 0.099 1.04


WI1 1.60–2.88 2.12* 0.28 0.65 13.4 0.057 0.012 1.28–2.76 2.00 0.26 0.17 12.9 0.057 0.024 1.06

WI2 1.89–3.40 2.52 0.36 0.58 14.4 0.061 0.057 1.67–3.69 2.45 0.33 0.79 13.4 0.056 0.057 1.03

WI3 2.42–4.21 3.48 0.41 0.36 11.7 0.052 0.026 2.51–4.11 3.38 0.35 0.22 10.4 0.046 0.007 1.03

WC1 3.80–5.62 4.63* 0.40 0.55 8.6 0.037 -0.077 3.69–5.32 4.49 0.33 0.10 7.3 0.032 -0.104 1.03

WP1 2.51–4.21 3.24 0.39 0.29 12.1* 0.051 0.028 2.45–4.08 3.16 0.30 0.44 9.5 0.042 -0.026 1.03

WP2 2.44–4.47 3.19* 0.40 0.10 12.4* 0.054 0.037 2.50–3.84 3.07 0.28 0.58 9.2 0.040 -0.039 1.04

WP3 2.70–4.41 3.39 0.36 0.12 10.6 0.045 -0.017 2.43–3.94 3.30 0.28 1.25 8.5 0.038 -0.057 1.03

WP4 2.63–4.28 3.34 0.34 0.21 10.3 0.044 -0.028 2.44–4.09 3.30 0.30 1.34 9.1 0.041 -0.038 1.01

WM1 2.18–3.95 2.84 0.33 0.02 11.6 0.049 -0.002 1.88–3.66 2.74 0.33 0.13 12.0 0.053 0.034 1.04


LI2 0.62–1.53 1.13 0.19 0.43 16.9 0.080 -0.002 0.68–1.82 1.07 0.20 0.66 18.5 0.080 0.038 1.05

LI3 1.05–2.34 1.63 0.27 0.66 16.8 0.073 0.040 1.06–2.35 1.56 0.26 0.31 16.5 0.073 0.058 1.05

LC1 3.97–6.13 4.98* 0.48 0.11 9.5 0.042 -0.028 3.48–5.79 4.80 0.43 0.06 9.0 0.040 -0.025 1.04

LP1 2.78–4.42 3.57* 0.38 0.14 10.6 0.046 -0.012 1.66–4.25 3.42 0.40 0.35 11.8 0.057 0.056 1.05

LP2 4.05–6.29 5.01* 0.51 0.08 10.3 0.045 0.008 3.82–6.11 4.80 0.46 0.18 9.5 0.042 -0.003 1.04

LP3 4.73–7.76 5.65* 0.58 0.03 10.3 0.043 0.024 4.32–6.57 5.45 0.49 0.20 9.1 0.040 -0.016 1.04

LP4 4.62–7.28 5.67 0.59 0.02 10.4 0.045 0.028 3.81–6.68 5.58 0.58 0.05 10.4 0.047 0.058 1.02

LM1 3.62–7.64 5.45 0.63 0.02 11.5 0.051 0.084 3.28–6.49 5.33 0.69 0.06 12.9 0.060 0.187 1.02


WI2 0.90–1.95 1.42 0.21 0.39 14.6 0.063 -0.009 0.89–2.06 1.44 0.21 0.72 14.8 0.065 0.024 0.98

WI3 1.22–2.94 1.75 0.28 0.58 15.9 0.067 0.037 1.21–2.37 1.77 0.23 0.57 12.7 0.056 0.009 0.99

WC1 3.26–5.13 4.01 0.37 0.58 9.3 0.040 -0.051 3.08–4.63 3.90 0.32 0.63 8.2 0.036 -0.067 1.03

WP1 2.22–3.75 2.86 0.33 0.15 11.7 0.050 0.002 1.48–3.47 2.76 0.30 0.28 10.9 0.051 0.006 1.03

WP2 2.79–4.27 3.49 0.35 0.06 10.1 0.044 -0.031 2.61–4.07 3.39 0.29 0.32 8.6 0.038 -0.054 1.03

WP3 2.87–4.57 3.61 0.37 0.17 10.1 0.044 -0.027 2.70–4.29 3.51 0.30 0.93 8.4 0.037 -0.060 1.03

WP4 2.88–4.54 3.52 0.35 0.10 9.8 0.042 -0.040 2.61–4.29 3.46 0.32 0.21 9.4 0.041 -0.027 1.02

WM1 2.53–4.16 3.14 0.33 0.14 10.5 0.045 -0.025 2.17–3.68 3.05 0.30 0.38 9.8 0.043 -0.021 1.03


that differ significantly (*P � 0.05; all P values exceed 0.001) from those of females according to Welch’s t-test (means) or Z-test (CVs) results. Statistical

abbreviations and symbols are explained in Table 1. Abbreviations for tooth lengths and widths are expanded in Table 4.




all species) in the toothrow (Figs 2B–2D, 3B–3D, 4B–4D and 5B–5D). Of a total of 10 incisorsize variables, six variables (WI1, WI2, LI2, WI2, LI3, and WI3) in one or both sexes of H. fas-ciata, five variables (LI3, WI3, LI2, LI3, and WI3) in one or both sexes of C. ursinus, four vari-ables (WI1, WI2, LI2, and LI3) in one or both sexes of P. largha, and one variable (LI3) in femaleE. jubatus had their CVs significantly higher than most CVs for the corresponding variables(lengths or widths, respectively) within the toothrow (Fig 9).

In comparison to the variation indices for other tooth classes, those for canines were high inC. ursinus, male E. jubatus, and mostly also in male P. largha; low in H. fasciata; and from lowto high in female E. jubatus and female P. largha. The canine indices varied from the lowest(CV, SDL, and RSD in female E. jubatus, female and male H. fasciata, and female P. largha) tothe highest (CV, SDL, and RSD in male E. jubatus and RSD in both sexes of C. ursinus and P.largha) in the toothrow (Figs 2B–2D, 3B–3D, 4B–4D and 5B–5D). CVs for LC1, LC1, and WC1

in female or male C. ursinus were significantly higher while those for WC1 in female E. jubatus

Fig 5. Arithmetic Mean and Variation Indices for Tooth Lengths andWidths Varied along the Toothrow and between Sexes in Phoca largha. A,arithmetic mean (mean); B, coefficient of variation (CV); C, standard deviation of log-transformed data (SDL); D, residual of standard deviation on arithmeticmean (RSD). Data from Table 9. Abbreviations for tooth lengths and widths are explained in Table 4.




and LC1, WC1, LC1, and WC1 in female or female and male H. fasciata were significantly lowerthan most CVs for other tooth lengths or widths, respectively, in the toothrow (Fig 9).

Table 9. Statistics for Tooth Lengths andWidths in Phoca largha.




LI1 1.74–2.43 2.06** 0.13 0.16 6.3 0.028 -0.024 1.61–2.27 1.96 0.13 0.31 6.4 0.028 -0.047 1.05

LI2 2.05–2.85 2.52* 0.17 0.83 6.8 0.030 -0.015 2.03–2.88 2.42 0.19 0.36 8.0 0.035 -0.003 1.04

LI3 3.27–4.51 3.84** 0.27 1.33 7.0 0.031 -0.010 2.77–4.36 3.63 0.26 1.12 7.3 0.032 0.004 1.06

LC1 6.82–10.66 8.25** 0.71 0.12 8.6* 0.037 0.115 6.38–8.66 7.49 0.50 0.29 6.7 0.029 0.044 1.10

LP1 4.64–7.54 5.82* 0.52 0.35 9.0* 0.038 0.100 4.76–7.10 5.60 0.39 0.74 6.9 0.029 0.026 1.04

LP2 7.08–10.29 8.17** 0.61 0.05 7.5 0.032 0.024 6.56–8.57 7.46 0.48 0.08 6.4 0.028 0.018 1.09

LP3 7.50–10.30 8.60** 0.62 0.05 7.2* 0.031 -0.000 7.12–9.00 8.11 0.44 0.20 5.4 0.024 -0.053 1.06

LP4 6.32–9.59 8.20** 0.59 0.02 7.2 0.032 -0.002 6.62–8.80 7.82 0.48 0.09 6.1 0.027 0.004 1.05

LM1 6.58–9.34 7.93** 0.57 0.10 7.2 0.031 -0.006 6.60–8.73 7.60 0.52 0.06 6.8 0.030 0.052 1.04


WI1 2.39–3.77 3.08** 0.30 0.44 9.6 0.042 0.069 2.25–3.36 2.74 0.21 1.38 7.8 0.034 0.001 1.12

WI2 2.78–4.59 3.61** 0.36 0.04 9.9 0.044 0.093 2.55–3.90 3.25 0.31 1.54 9.6 0.042 0.072 1.11

WI3 3.58–5.96 5.15** 0.38 1.92 7.5 0.034 0.010 3.94–5.47 4.67 0.36 0.45 7.8 0.034 0.049 1.10

WC1 5.07–8.10 6.95** 0.51 0.23 7.3 0.033 0.007 5.44–7.17 6.32 0.37 0.15 5.9 0.026 -0.025 1.10

WP1 3.32–4.77 4.00** 0.28 0.33 7.1 0.031 -0.008 3.27–4.34 3.75 0.26 0.32 7.1 0.030 -0.001 1.07

WP2 3.56–5.41 4.40** 0.33 0.16 7.6 0.033 0.014 3.50–4.54 4.06 0.25 0.58 6.1 0.027 -0.034 1.08

WP3 3.80–5.28 4.63** 0.28 0.28 6.1 0.027 -0.056 3.56–4.97 4.27 0.31 0.14 7.2 0.031 0.014 1.08

WP4 3.94–5.37 4.72** 0.28 0.37 6.0 0.026 -0.062 3.72–5.01 4.41 0.29 0.45 6.6 0.029 -0.009 1.07

WM1 3.77–5.22 4.51** 0.32 0.16 7.0 0.031 -0.013 3.60–5.01 4.24 0.31 0.10 7.3 0.032 0.017 1.06


LI2 1.68–2.29 1.92* 0.15 0.42 7.8 0.033 0.006 1.59–2.31 1.87 0.15 0.20 7.9 0.034 -0.020 1.03

LI3 2.07–2.93 2.57* 0.21 0.42 8.0 0.035 0.016 1.85–3.10 2.47 0.20 1.31 8.0 0.036 -0.001 1.04

LC1 5.84–9.19 7.53** 0.55 0.96 7.3 0.032 0.003 5.72–7.61 6.89 0.46 0.65 6.7 0.030 0.036 1.09

LP1 4.49–6.62 5.48** 0.39 0.98 7.0 0.030 -0.012 4.44–6.00 5.15 0.37 0.59 7.2 0.031 0.032 1.06

LP2 7.07–9.76 8.22** 0.58 0.10 7.1 0.030 -0.013 6.74–8.97 7.74 0.47 0.13 6.1 0.027 -0.001 1.06

LP3 7.79–10.42 9.08** 0.62 0.20 6.8 0.030 -0.035 7.40–9.85 8.49 0.49 0.01 5.7 0.025 -0.026 1.07

LP4 7.16–10.02 8.62** 0.59 0.02 6.8 0.030 -0.035 7.18–9.25 8.13 0.45 0.18 5.6 0.024 -0.042 1.06

LM1 8.08–10.96 9.35** 0.65 0.02 7.0 0.031 -0.020 7.68–9.82 8.90 0.50 0.45 5.6 0.024 -0.035 1.05


WI2 1.79–2.68 2.17** 0.17 0.37 8.0 0.035 0.012 1.75–2.61 2.01 0.15 1.38 7.7 0.033 -0.021 1.08

WI3 2.22–3.09 2.60** 0.18 0.64 7.1 0.031 -0.008 1.99–2.86 2.41 0.17 0.65 7.0 0.031 -0.026 1.08

WC1 5.18–7.60 6.21** 0.44 0.52 7.2 0.031 -0.005 4.98–6.35 5.63 0.33 2.23 5.8 0.025 -0.036 1.10

WP1 3.46–4.67 3.96** 0.27 0.64 6.7 0.029 -0.024 2.88–4.24 3.69 0.28 1.22 7.5 0.033 0.013 1.07

WP2 4.09–5.55 4.78** 0.33 0.42 6.9 0.030 -0.020 3.80–5.14 4.47 0.30 0.83 6.7 0.029 -0.002 1.07

WP3 4.10–5.61 4.90** 0.31 0.19 6.4 0.028 -0.044 3.79–5.20 4.55 0.31 2.53 6.8 0.030 0.001 1.08

WP4 4.03–5.46 4.67** 0.30 0.11 6.5 0.029 -0.035 3.69–4.98 4.35 0.28 1.38 6.4 0.028 -0.017 1.07

WM1 3.75–5.29 4.68** 0.32 0.51 6.8 0.030 -0.022 3.60–5.03 4.34 0.31 0.24 7.2 0.032 0.017 1.08







The variation indices for postcanines mostly tended to progressively increase or decreasefrom the first premolar to the last molar or decrease from both the first premolar and lastmolar to one of the intermediary postcanines. These indices varied from the lowest (CV, SDL,and RSD in C. ursinus, E. jubatus, and P. largha) to the highest (CV, SDL, and RSD in all spe-cies) in the toothrow (Figs 2B–2D, 3B–3D, 4B–4D and 5B–5D). CV for LM2 significantlyexceeded all other CVs for tooth lengths within the toothrow in both sexes of C. ursinus. CVsfor two other variables (LP1 andWM2) in female C. ursinus, two variables (LM1 and LP2) inmale E. jubatus, and six variables (WM1, LP1, WP1, LP2, LP3, and LM1) in female H. fasciatadiffered significantly from most CVs for other tooth lengths or widths, respectively, in thetoothrow (Fig 9).

CV and SDL were significantly correlated with mean variable size only inH. fasciata andfemale P. largha. There was a significant positive correlation between CV and both SDL andRSD (Table 10). The weakest relationship between CV and RSD was observed in male H.

Fig 6. Arithmetic Mean and Variation Indices for Tooth Lengths andWidths Varied along the Toothrow and among Male Pinniped Species. A,arithmetic mean (mean); B, coefficient of variation (CV); C, standard deviation of log-transformed data (SDL); D, residual of standard deviation on arithmeticmean (RSD). Data from Tables 6–9. Abbreviations for tooth lengths and widths are explained in Table 4.




fasciata (r = 0.52), female H. fasciata (r = 0.67), and female P. largha (r = 0.60). However, whenthe incisor variables were excluded from the comparison, r for this relationship increased to0.89 in male H. fasciata, 0.98 in female H. fasciata, and 0.68 in female P. largha, all of these val-ues being highly significant at P< 0.0003 according to Student’s t-test results.

Plotting RSD against mean variable size revealed outliers from an otherwise normal distri-bution in both sexes of C. ursinus (LM2) and male P. largha (WI2, LC1, and LP1). No such outli-ers occurred in female P. largha and either sex of E. jubatus andH. fasciata (Fig 10).

Sexual dimorphismAll mean variables were significantly higher in males than in females in C. ursinus, E. jubatus,and P. largha (Tables 6, 7 and 9). InH. fasciata, 10 mean variables were significantly higherand 22 mean variables were insignificantly higher in males, whereas two mean variables (WI2andWI3) were insignificantly higher in females (Table 8). Most variables had their CVs higher

Fig 7. Arithmetic Mean and Variation Indices for Tooth Lengths andWidths Varied along the Toothrow and among Female Pinniped Species. A,arithmetic mean (mean); B, coefficient of variation (CV); C, standard deviation of log-transformed data (SDL); D, residual of standard deviation on arithmeticmean (RSD). Data from Tables 6–9. Abbreviations for tooth lengths and widths are explained in Table 4.




in males than in females in all species (Figs 2B, 3B, 4B and 5B), although the CVs of males andfemales differed significantly for only five variables in E. jubatus (Table 7) and three variablesin C. ursinus (Table 6),H. fasciata (Table 8), and P. largha (Table 9). SDLs were also mostlyhigher in males than in females in all species (Figs 2C, 3C, 4C and 5C). RSDs were mostlyhigher in males than in females in E. jubatus (Fig 3D), as frequently higher as lower in malesthan in females in C. ursinus (Fig 2D), and mostly lower in males than in females in H. fasciataand P. largha (Figs 4D and 5D).

M/Fs ranged 1.05–1.76 in C. ursinus (Table 6), 1.07–1.82 in E. jubatus (Table 7), 0.98–1.06inH. fasciata (Table 8), and 1.03–1.12 in P. largha (Table 9). Most variables had the highest M/F in E. jubatus, the second highest in C. ursinus, the third highest in P. largha, and the lowest inH. fasciata. When M/Fs were compared within species, the M/Fs of canines were highest andthose of I3 second highest in C. ursinus and E. jubatus but not in H. fasciata and P. largha,where the M/Fs of canines were within the 19 and eight highest M/Fs, respectively, and the M/Fs of I3 were within the 25 and 26 highest, respectively (Tables 6–9).

There was a significant positive correlation betweenM/F and mean variable size in C. ursinusand E. jubatus but not inH. fasciata and P. largha (Table 10). There was a moderate but significantpositive correlation betweenM/F and CV in male C. ursinus and male E. jubatus, betweenM/Fand SDL in male P. largha, and betweenM/F and RSD in both sexes of C. ursinus andmale E. juba-tus. The weakest relationship betweenM/F and the variation indices was inH. fasciata (Table 10).

Effect of tooth eruption sequenceThere was a significant positive correlation between the sequence of tooth eruption and bothmean and SD for the lengths of teeth in C. ursinus but not for the widths. There was no signifi-cant correlation between the tooth eruption sequence and CV, SDL, RSD, or M/F (Table 11).The variation indices were not progressively higher when ordered according to the sequence oftooth eruption (Fig 8).

Discussion and Conclusions

Reliability and usefulness of variation indicesAlthough variable size ranged widely in our study, most MEs were low (<0.5%) and there wasmostly no significant negative correlation between CV and mean variable size. CV, SDL, and

Table 10. Pearson’s Product Moment Correlation Coefficients and Their Statistical Significance among the Arithmetic Mean, Measurement Error,and Variation and Sexual Dimorphism Indices for Tooth Lengths andWidths in Pinniped Species.

Comparison Callorhinus ursinus Eumetopias jubatus Histriophoca fasciata Phoca largha

Males Females Males Females Males Females Males Females

mean–ME -0.10 -0.30 -0.07 -0.23 -0.62** -0.37* -0.31 -0.38*

mean–CV 0.03 -0.21 0.06 -0.20 -0.76** -0.61** -0.10 -0.71**

mean–SDL 0.00 -0.20 0.03 -0.19 -0.76** -0.57** -0.13 -0.70**

mean–M/F 0.75** 0.42* 0.75** 0.37* -0.01 -0.04 0.05 0.00

CV–SDL 0.99** 0.99** 0.99** 0.99** 0.99** 0.99** 0.99** 1.00**

CV–RSD 0.97** 0.96** 0.96** 0.95** 0.52* 0.67** 0.93** 0.60**

CV–M/F 0.36* 0.24 0.34* -0.09 -0.03 0.05 0.33 0.11

SDL–M/F 0.29 0.20 0.29 -0.12 0.03 0.05 0.35* 0.12

RSD–M/F 0.39* 0.38* 0.36* 0.01 -0.00 -0.03 0.31 0.24

Statistically significant coefficients according to Student’s t-test results are indicated by asterisks (*P � 0.05, **P � 0.001). Abbreviations are explained in

Table 1.




the size-independent RSD varied similarly along the toothrow and were significantly correlatedin all species. These results suggest that in most cases CV measured variation reliably.

In all species, CV and SDL showed similar levels of correlation with mean variable size, var-ied almost identically along the toothrow, and were very strongly correlated with each other(r = 0.99–1.00). This agrees with previous observations from land carnivorans [13–15] and sug-gests the redundancy of SDL with CV.

Even though independent of size and apparently mostly reliable, RSD was not fully reliablein both sexes of C. ursinus and male P. largha, as indicated by outliers from an otherwise nor-mal distribution in the plots of this index against mean variable size. This problem of RSD waspreviously noticed by Polly [12], who argued that such outliers caused RSDs of large teeth toappear artificially low. Because such outliers represent relatively highly variable variables, we

Fig 8. Variation Indices for Tooth Lengths andWidths Varied according to the Tooth Eruption Sequence in Pooled Sexes of Callorhinus ursinus. A,coefficient of variation (CV); B, standard deviation of log-transformed data (SDL); C, residual of standard deviation on arithmetic mean (RSD). Variables areordered according to the sequence of tooth eruption [47] from the first (left) to the last (right) erupting tooth. Numbers at dots are the values of indices for thecorresponding variables. Abbreviations for tooth lengths and widths are explained in Table 4.




conclude that RSD can reliably measure variation when all variables are similarly variable, butthis index may be misleading when one or more variables are markedly more variable than oth-ers. Another drawback that reduces the utility of RSD for measuring variation is that in con-trast to CV and SDL, RSD is not comparable between different groups of organisms (e.g.,species or sexes) if obtained from different regression analyses and that the way how RSD iscalculated covers potential differences in variation between the compared groups of organisms(RSDs from each regression analysis are both positive and negative and center around zero).

Tooth size variation in pinnipedsDifferential variation along the toothrow and among species. Contrary to the hypothe-

sis of Polly [12] that size variation among mammalian teeth is relatively homogeneous bothwithin and among species except highly variable canines in some species, our results show thatsize variation among pinniped teeth can considerably differ both within and among species.Even though this variation was relatively homogeneous in P. largha, it was clearly heteroge-neous in C. ursinus, E. jubatus, and H. fasciata. Not only canines but also incisors were rela-tively highly variable in most cases although the canines of H. fasciata were less variable thanother teeth of the toothrow. Incisor and canine variables were partly difficult to measure,which could result in artificial inflation of their variation indices, but any relevant contributionfrom this potential source was not supported by the MEs of these variables, which were mostlylower than 1%. Moreover, differences in size variation were observed among postcanines.Probably most remarkable is the relatively high variation in the size of the most distal upperpostcanines in both otariids, C. ursinus (M2) and E. jubatus (M1).

Our results from CV and SDL indicate that the dentition ofH. fasciata is the most variablein size, that of E. jubatus is the least variable, and those of C. ursinus and P. largha are at inter-mediate levels of the overall size variation. Admittedly, there was a significant negative correla-tion between CV and mean variable size in both sexes ofH. fasciata and female P. largha,which suggests that the values of this index might be artificially inflated in these species due tothe size-related bias revealed by Polly [12]. However, contrary to this suggestion, CV wasmostly lower in females than in males in both species although all (P. largha) or almost all (H.fasciata) mean variables were higher in males than in females. Furthermore, there was no sig-nificant negative correlation between CV and mean variable size in male P. largha, C. ursinus,or E. jubatus.

A comparison of CVs for the lengths of lower postcanines between Pagophilus groenlandi-cus (6.6–8.8% [40]) and H. fasciata (9.1–12.9%) suggests that the dentition of the former spe-cies is less variable in size. The CVs of 9.9% (males) and 9.5% (females) reported for the lengthof P3 in Pusa hispida [40] are similar to those inH. fasciata (10.3 and 9.1%, respectively). Inturn, CVs for the length and width of C1 recorded from male Antarctic (Arctophoca gazella;5.7% and 8.0%, respectively) and subantarctic (Arctophoca tropicalis; 8.1% and 8.8%, respec-tively) fur seals [49] are similar to or lower than those in the males of species examined here(8.0–9.4% and 7.2–8.9%, respectively).

Sexual dimorphism. Our results indicate that sexual size dimorphism is the most pro-nounced for the dentition of E. jubatus, the second most pronounced for the dentition of C.ursinus, the third most pronounced for the dentition of Phoca largha, and the least pronouncedfor the dentition ofH. fasciata, with teeth being, on average, larger in males than in females in

Fig 9. Statistical Significance of Pairwise Differences between the Coefficients of Variation for Tooth Lengths or Widths within the Toothrow inPinniped Species. P values come from the Z-test. The coefficients of variation are shown in Tables 6–9. Abbreviations for tooth lengths and widths areexplained in Table 4.




all species. Miller et al. [40] reported that the lower postcanines of Pagophilus groenlandicusand P3 of Pusa hispida were, on average, also larger in males. It has also been noted that thecanines of the northern and southern elephant seals (Mirounga angustirostris andM. leonina)were larger in males [50–52].

The canines and, to a lesser degree, I3 were the most sexually dimorphic teeth in C. ursinusand E. jubatus, where the observed ranges of canine variables did not overlap between sexes.The canines of these species were larger and more sexually dimorphic relative to other teeththan those ofH. fasciata and Phoca largha. Moreover, there was a positive relation betweensexual dimorphism and tooth size in both otariids, but no such a relationship was observed inthe two phocids.

Comparison with nonpinniped carnivoransA comparison of how the size of teeth changes with position along the toothrow between pin-nipeds and other carnivorans (Fig 11) shows that the incisors and canines exhibit a similar var-iation, whereas the postcanines exhibit a different variation. Unlike the postcanines of landcarnivorans, the pinniped postcanines are mostly very similar in size and, as indicated by ourmeasurements, some can vary in sequence according to size within species.

Contrary to the hypothesis of Miller et al. [40] that the postcanines of pinnipeds are morevariable in size than those of land carnivorans due to evolutionary simplification of morphol-ogy, our results indicate that the pinniped dentitions represent a wide spectrum of the levels ofsize variation ranging from a relatively low variation as in land carnivorans to a high variation(Fig 12). Furthermore, although the postcanines of both otariids were mostly simpler in formthan those of the phocids (Fig 1), the latter were mostly more variable in size (Fig 12).

Fig 10. Relationship between the Residual of Standard Deviation on Arithmetic Mean (RSD) and theArithmetic Mean (mean) for Tooth Lengths andWidths in Pinniped Species.Data from all teeth (Tables6–9). Inset numbers represent the results of the Shapiro–Wilk test (W) and, under this test, the probability ofwrongly rejecting the null hypothesis that the data are normally distributed (P). Numbers in parentheses referto all data except outliers from an otherwise normal distribution. These outliers are highlighted in red andlabeled with the variable abbreviation (explained in Table 4).


Table 11. Spearman’s Rank Correlation Coefficients and Their Statistical Significance between the Sequence of Tooth Eruption and the ArithmeticMean, Standard Deviation, and Variation and Sexual Dimorphism Indices for Tooth Lengths andWidths inCallorhinus ursinus.

Comparison Tooth lengths Tooth widths

Males Females Males andfemales

Males Females Males andfemales

rs P rs P rs P rs P rs P rs P

Eruption sequence–mean 0.74* 0.000 0.76* 0.000 0.75* 0.000 0.17 0.487 0.32 0.197 0.25 0.310

Eruption sequence–SD 0.66* 0.004 0.88* 0.000 0.67* 0.003 0.02 0.928 0.40 0.104 -0.18 0.482

Eruption sequence–CV 0.12 0.638 0.21 0.398 0.32 0.197 -0.05 0.831 0.04 0.876 -0.18 0.462

Eruption sequence–SDL 0.12 0.621 0.23 0.366 0.32 0.191 -0.07 0.799 0.04 0.869 -0.16 0.530

Eruption sequence–RSD -0.06 0.805 0.29 0.242 -0.23 0.357 -0.06 0.824 0.11 0.668 -0.01 0.967

Eruption sequence–M/F 0.39 0.110 0.39 0.110 0.39 0.110 -0.26 0.294 -0.26 0.294 -0.26 0.294

The sequence of tooth eruption follows Scheffer and Kraus [47] and is: I2, I1, I3, I

2, P1, P1, I3, P2, P

2, P3, P4, P3, P4, M1, C1, C

1, M1, and M2 (tooth symbols

expanded in Table 5). Statistically significant coefficients at P � 0.05 are indicated by an asterisk. P values derive from algorithm AS 89 [48]. Statistical

abbreviations and symbols are explained in Table 1.




Testing hypotheses that explain differential size variation along thetoothrow

The hypothesis invoking relative tooth position in a developmental field. Our resultshave not shown a consistent pattern to support this hypothesis. Whereas some of the results fitthe predictions of the hypothesis (e.g., all variation indices for the lengths of upper teeth inmale E. jubatus progressively increased in value from the central part to the mesial and distalends of the postcanine toothrow; Fig 3B–3D), other results do not (e.g., all variation indices forthe lengths of upper teeth in female C. ursinus progressively increased in value from the mesialto the distal end of the postcanine toothrow; Fig 2B–2D).

The hypothesis invoking relative tooth occlusal complexity. According to this hypothe-sis, the level of size variation in teeth is inversely proportional to their occlusal complexity [20].This means that teeth that have similar occlusal complexity should be similarly variable in size.Our findings mostly negate this prediction. Even though teeth with similar occlusal complexityin most cases showed a similar size variation in Phoca largha, such teeth in most cases differedin size variation in C. ursinus, E. jubatus, and H. fasciata.

The hypothesis invoking the relative timing of tooth formation and sexually dimorphichormonal activity. Our results do not support this hypothesis. In C. ursinus we have found

Fig 11. Arithmetic Mean for Tooth Lengths andWidths Varied along the Toothrow and among Pinniped and Other Carnivoran Species. A, upperteeth; B, lower teeth. Lengths are mesiodistal, widths are vestibulolingual. Tooth symbols are explained in Table 5. Family affiliations are indicated fornonpinniped species. Arithmetic mean (mean) values are averaged between sexes based on data from this study (pinnipeds) and previous investigations(Lycalopex gymnocercus, pampas fox [F. J. Prevosti, pers. comm., 26 February 2013]; Vulpes vulpes, red fox [13];Meles meles, European badger [25])except for P1 and P1 ofM.meles, where the values are from females [53].




neither a significant positive correlation between the sequence of tooth eruption and CV, SDL,or RSD nor a significant relationship between this sequence and M/F, and the teeth orderedaccording to the eruption sequence have not shown progressively higher variation indices forpooled males and females.

AcknowledgmentsWe would like to thank Tetsuya Amano and Noriyuki Ohtaishi (HUM), Masaru Kato andFumihito Takaya (HUNHM), Mari Kobayashi (TUA), and Naoki Kohno and Tadasu K.Yamada (NSMT) for access to collections in their respective institutions. We also thank Fran-cisco Prevosti for sharing unpublished data from male and female Lycalopex gymnocercus andhelpful discussions of statistical issues.

Author ContributionsConceived and designed the experiments: MW. Performed the experiments: MW. Analyzedthe data: SS MW. Contributed reagents/materials/analysis tools: MAMM SS MW.Wrote thepaper: MW.

Fig 12. Coefficient of Variation for Tooth Lengths andWidths Varied along the Toothrow and among Pinniped and Other Carnivoran Species. A,upper teeth; B, lower teeth. Lengths are mesiodistal, widths are vestibulolingual. Tooth symbols are explained in Table 5. Family affiliations are indicated fornonpinniped species. Coefficient of variation (CV) values are averaged between sexes based on data from this study (pinnipeds) and previous investigations(Lycalopex gymnocercus [F. J. Prevosti, pers. comm., 25 October 2012], Vulpes vulpes [13],Meles meles [25]) except for P1 and P1 ofM.meles, where CVsare from females [53]. For CVs from other land carnivoran species or other populations of the same land carnivoran species, see [12, 15, 16, 21, 24, 32, 36,54–60]. Note that CVs based on pooled sexes [12, 14, 16, 21, 36, 54, 55, 59] can be higher than for either sex separately (they are totally or mostly higherwhen derived from sexually dimorphic species; compare CVs in Table 6 and Fig 8) and therefore comparing them directly with our averaged CVs can bemisleading.




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